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Fasciolosis, a foodborne zoonotic trematode infection in cattle in Bangladesh: multifaceted validation of parthenogenecity and anthelmintic efficacy
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DOI：10.1051/parasite/2026004.png)
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Abstract
En 中文
Parthenogenic Fasciola (Trematoda: Fasciolidae) flukes have been developed by the hybridization of Fasciola hepatica and Fasciola gigantica. They are aspermic (asF) but capable of clonal expansion through parthenogenesis and are spreading rapidly throughout the globe. Here, we unambiguously prove the occurrence of parthenogenic Fasciola in cattle in Bangladesh, along with their ex vivo culture protocol and anthelmintic efficacy. By employing multiple conventional and molecular tools, we confirmed the presence of both the spermic F. gigantica (sFg) (31.7%; 814/2575) and asF (68.3%; 1761/2575) in Bangladesh. Both the adult sFg and asF survived well in DMEM supplemented with 20% bovine serum and 20% bovine bile. Using a DMEM-based ex vivo culture protocol, we found that nitroxynil (NTX) and oxyclozanide (OCZ) efficiently killed both sFg and asFg in a concentration and time-dependent manner. Surprisingly, triclabendazole (TCBZ) and clorsulon (CRL) killed neither sFg nor asF. Also, praziquantel, albendazole, and levamisole did not affect the viability of the flukes. We found that all TCBZ survivors had more than one mutation, both in nucleotides (G440A, G643A, and G788A) and amino acids (R147K, E215K, and R263K) of the binding pocket of carboxylesterase B (CestB), providing molecular evidence of TCBZ resistance in Fasciola. Taken together, asF constitutes more than two-thirds of the Fasciola population in Bangladesh. This study unambiguously proved the ineffectiveness of TCBZ against both asF and sFg circulating in Bangladesh. Therefore, only OCZ and NTX remain effective against fasciolosis, which thus poses ongoing public health risks of infection in humans with TCBZ-tolerant strains of fasciolosis. Les douves Fasciola parth & eacute;nog & eacute;niques (Trematoda : Fasciolidae) sont issues de l'hybridation de Fasciola hepatica et Fasciola gigantica ; elles sont aspermiques (asF), capables de se multiplier par parth & eacute;nog & eacute;n & egrave;se et se propagent rapidement & agrave; travers le monde. Dans cette & eacute;tude, nous d & eacute;montrons sans ambigu & iuml;t & eacute; la pr & eacute;sence de Fasciola parth & eacute;nog & eacute;n & eacute;tique chez les bovins au Bangladesh, et d & eacute;crivons son protocole de culture ex vivo ainsi que l'efficacit & eacute; des anthelminthiques. Gr & acirc;ce & agrave; l'utilisation de plusieurs outils conventionnels et mol & eacute;culaires, nous avons confirm & eacute; la pr & eacute;sence de F. gigantica spermatique (sFg) (31,7 % ; 814/2575) et asF (68,3 % ; 1761/2575) au Bangladesh. Les douves adultes sFg et asF ont toutes deux bien surv & eacute;cu dans du DMEM suppl & eacute;ment & eacute; avec 20 % de s & eacute;rum bovin et 20 % de bile bovine. Gr & acirc;ce & agrave; un protocole de culture ex vivo en milieu DMEM, nous avons constat & eacute; que le nitroxynil (NTX) et l'oxyclosanide (OCZ) tuaient efficacement les deux types de douves, de mani & egrave;re concentration-d & eacute;pendante et temps-d & eacute;pendante. De fa & ccedil;on surprenante, le triclabendazole (TCBZ) et le clorsulon (CRL) n'ont eu aucun effet sur les deux esp & egrave;ces. Par ailleurs, le praziquantel, l'albendazole et le l & eacute;vamisole n'ont pas affect & eacute; la viabilit & eacute; des douves. Nous avons constat & eacute; que tous les survivants au TCBZ pr & eacute;sentaient plusieurs mutations, tant au niveau des nucl & eacute;otides (G440A, G643A et G788A) que des acides amin & eacute;s (R147K, E215K et R263K) du site de liaison de la carboxylest & eacute;rase B (CestB), ce qui constitue une preuve mol & eacute;culaire de la r & eacute;sistance au TCBZ chez Fasciola. La souche asF repr & eacute;sente plus des deux tiers de la population de Fasciola au Bangladesh. Cette & eacute;tude a d & eacute;montr & eacute; sans ambigu & iuml;t & eacute; l'inefficacit & eacute; du TCBZ contre les souches asF et sFg circulant au Bangladesh. Par cons & eacute;quent, seuls l'OCZ et le NTX restent efficaces contre la fasciolose, ce qui repr & eacute;sente un risque persistant pour la sant & eacute; publique li & eacute; & agrave; l'infection humaine par des souches de fasciolose tol & eacute;rantes au TCBZ.
Keywords:
Fasciola gigantica
Parthenogenic Fasciola
Liver fluke
Carboxylesterase B mutation
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